Skip to main content
SpringerLink
Log in

A survey of cellulose microfibril patterns in dividing, expanding, and differentiating cells of Arabidopsis thaliana

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Cellulose microfibrils are critical for plant cell specialization and function. Recent advances in live cell imaging of fluorescently tagged cellulose synthases to track cellulose synthesis have greatly advanced our understanding of cellulose biosynthesis. Nevertheless, cellulose deposition patterns remain poorly described in many cell types, including those in the process of division or differentiation. In this study, we used field emission scanning electron microscopy analysis of cryo-planed tissues to determine the arrangement of cellulose microfibrils in various faces of cells undergoing cytokinesis or specialized development, including cell types in which cellulose cannot be imaged by conventional approaches. In dividing cells, we detected microfibrillar meshworks in the cell plates, consistent with the concentration at the cell plate of cellulose synthase complexes, as detected by fluorescently tagged CesA6. We also observed a loss of parallel cellulose microfibril orientation in walls of the mother cell during cytokinesis, which corresponded with the loss of fluorescently tagged cellulose synthase complexes from these surfaces. In recently formed guard cells, microfibrils were randomly organized and only formed a highly ordered circumferential pattern after pore formation. In pit fields, cellulose microfibrils were arranged in circular patterns around plasmodesmata. Microfibrils were random in most cotyledon cells except the epidermis and were parallel to the growth axis in trichomes. Deposition of cellulose microfibrils was spatially delineated in metaxylem and protoxylem cells of the inflorescence stem, supporting recent studies on microtubule exclusion mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

CSC:

Cellulose synthase complex

FESEM:

Field emission scanning electron microscopy

YFP:

Yellow fluorescent protein

References

  • Akkerman M, Franssen-Verheijen MA, Immerzeel P, Hollander LD, Schel JH, Emons AM (2012) Texture of cellulose microfibrils of root hair cell walls of Arabidopsis thaliana, Medicago truncatula, and Vicia sativa. J Microsc 247:60–67

    Article  PubMed  CAS  Google Scholar 

  • Anderson CT, Carroll A, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152:787–796

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Baluska F, Liners F, Hlavacka A, Schlicht M, Van Cutsem P, McCurdy DW, Menzel D (2005) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225:141–155

    Article  PubMed  CAS  Google Scholar 

  • Baskin T, Beemster G, Judy-March J, Marga F (2004) Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis. Plant Physiol 135:2279–2290

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Baskin TI, Meekes H, Liang BM, Sharp RE (1999) Regulation of growth anisotropy in well-watered and water-stressed maize roots. II. Role of cortical microtubules and cellulose microfibrils. Plant Physiol 119:681–692

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Burk DH, Ye ZH (2002) Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein. Plant Cell 14:2145–2160

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Busby CH, Gunning BES (1984) Microtubules and morphogenesis in stomata of the water fern Azolla: an unusual mode of guard cell and pore development. Protoplasma 122(1–2):108–119

    Article  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants—consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  PubMed  CAS  Google Scholar 

  • Crowell EF, Timpano H, Desprez T, Franssen-Verheijen T, Emons AM, Hofte H, Vernhettes S (2011) Differential regulation of cellulose orientation at the inner and outer face of epidermal cells in the Arabidopsis hypocotyl. Plant Cell 23:2592–2605

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fisher DD, Cyr RJ (1998) Extending the microtubule/microfibril paradigm—cellulose synthesis is required for normal cortical microtubule alignment in elongating cells. Plant Physiol 116:1043–1051

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fujita M, Himmelspach R, Hocart CH, Williamson RE, Mansfield SD, Wasteneys GO (2011) Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis. Plant J 66:915–928

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Himmelspach R, Ward J, Whittington A, Hasenbein N, Liu C, Truong TT, Galway ME, Mansfield SD, Hocart CH, Wasteneys GO (2013) The anisotropy1 D604N mutation in the Arabidopsis cellulose synthase1 catalytic domain reduces cell wall crystallinity and the velocity of cellulose synthase complexes. Plant Physiol 162:74–85

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fujita M, Lechner B, Barton DA, Overall RL, Wasteneys GO (2012) The missing link: do cortical microtubules define plasma membrane nanodomains that modulate cellulose biosynthesis? Protoplasma 249:59–67

    Article  CAS  Google Scholar 

  • Galatis P (1980) Microtubules and guard cell morphogenesis in Zea mays L. J Cell Sci 45:211–244

    PubMed  CAS  Google Scholar 

  • Green PB, King A (1966) A mechanism for origin of specifically oriented textures in development with special reference to nitella wall texture. Aust J Biol Sci 19:421–438

    Google Scholar 

  • Hardham AR, Green PB, Lang JM (1980) Reorganization of cortical microtubules and cellulose deposition during leaf formation in Graptopetalum paraguayense. Planta 149:181–195

    Article  PubMed  CAS  Google Scholar 

  • Himmelspach R, Williamson RE, Wasteneys GO (2003) Cellulose microfibril alignment recovers from DCB-induced disruption despite microtubule disorganization. Plant J 36:565–575

    Article  PubMed  CAS  Google Scholar 

  • Kakimoto M, Shibaoka H (1992) Synthesis of polysaccharides in phragmoplasts isolated from Tobacco BY-2 cells. Plant Cell Physiol 33:353–361

    CAS  Google Scholar 

  • Kerstens S, Verbelen JP (2003) Cellulose orientation at the surface of the Arabidopsis seedling. Implications for the biomechanics in plant development. J Struct Biol 144:262–270

    Article  PubMed  CAS  Google Scholar 

  • Lucas JR, Nadeau JA, Sack FD (2006) Microtubule arrays and Arabidopsis stomatal development. J Exp Bot 57:71–79

    Google Scholar 

  • MacKinnon I, Sturcova A, Sugimoto-Shirasu K, His I, McCann M, Jarvis M (2006) Cell-wall structure and anisotropy in procuste, a cellulose synthase mutant of Arabidopsis thaliana. Planta 224:438–448

    Article  PubMed  CAS  Google Scholar 

  • Marga F, Grandbois M, Cosgrove DJ, Baskin TI (2005) Cell wall extension results in the coordinate separation of parallel microfibrils: evidence from scanning electron microscopy and atomic force microscopy. Plant J 43:181–190

    Article  PubMed  CAS  Google Scholar 

  • Moore PJ, Staehelin LA (1988) Immunogold localization of the cell-wall-matrix polysaccharides rhamnogalacturonan I and xyloglucan during cell expansion and cytokinesis in Trifolium pratense L.—implication for secretory pathways. Planta 174:433–445

    Article  PubMed  CAS  Google Scholar 

  • Mueller SC, Brown RM (1982a) The control of cellulose microfibril deposition in the cell wall of higher plants. II. Freeze-fracture microfibril patterns in maize seedling tissues following experimental alteration with colchicine and ethylene. Planta 154:501–515

    Article  PubMed  CAS  Google Scholar 

  • Mueller SC, Brown RMJ (1982b) The control of cellulose microfibril deposition in the cell wall of higher plants. I. Can directed membrane flow orient cellulose microfibrils? Indirect evidence from freeze-fractured plasma membranes of maize and pine seedlings. Planta 154:489–500

    Article  PubMed  CAS  Google Scholar 

  • Oda Y, Fukuda H (2012) Secondary cell wall patterning during xylem differentiation. Curr Opin Plant Biol 15:38–44

    Article  PubMed  CAS  Google Scholar 

  • Oda Y, Iida Y, Kondo Y, Fukuda H (2010) Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr Biol 20:1197–1202

    Article  PubMed  CAS  Google Scholar 

  • Oda Y, Mimura T, Hasezawa S (2005) Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol 137:1027–1036

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pagant S, Bichet A, Sugimoto K, Lerouxel O, Desprez T, McCann M, Lerouge P, Vernhettes S, Hofte H (2002) KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14:2001–2013

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Palevitz BA, Hepler PK (1976) Cellulose microfibril orientation and cell shaping in developing guard cells of Allium—role of microtubules and ion accumulation. Planta 132:71–93

    Article  PubMed  CAS  Google Scholar 

  • Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495

    Article  PubMed  CAS  Google Scholar 

  • Pesquet E, Korolev AV, Calder G, Lloyd CW (2010) The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 20:744–749

    Article  PubMed  CAS  Google Scholar 

  • Preston R (1974) The physical biology of plant cell walls. Chapman and Hall, London

    Google Scholar 

  • Probine MC, Preston RD (1962) Cell growth and structure and mechanical properties of wall in internodal cells of Nitella opaca. 2. Mechanical properties of walls. J Exp Bot 13:111–127

    Article  CAS  Google Scholar 

  • Refregier G, Pelletier S, Jaillard D, Hofte H (2004) Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiol 135:959–968

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Richmond P (1983) Patterns of cellulose microfibril deposition and rearrangement in Nitella: in vivo analysis by a birefringence index. J Appl Polym Sci 37:107–122

    CAS  Google Scholar 

  • Richmond P, Metraux J, Taiz L (1980) Cell expansion patterns and directionality of wall mechanical properties in Nitella. Plant Physiol 65(2):211–217

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Samuels A, Giddings T, Staehelin L (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357

    Article  PubMed  CAS  Google Scholar 

  • Singh AP, Srivasta LM (1973) Fine structure of pea stomata. Protoplasma 76:61–82

    Article  Google Scholar 

  • Sugimoto K, Himmelspach R, Williamson RE, Wasteneys GO (2003) Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15:1414–1429

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sugimoto K, Williamson RE, Wasteneys GO (2000) New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol 124:1493–1506

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sugimoto K, Williamson RE, Wasteneys GO (2001) Wall architecture in the cellulose-deficient rsw1 mutant of Arabidopsis thaliana: microfibrils but not microtubules lose their transverse alignment before microfibrils become unrecognizable in the mitotic and elongation zones of roots. Protoplasma 215:172–183

    Article  PubMed  CAS  Google Scholar 

  • Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol Plant Mol Biol 35

  • Talbot MJ, Wasteneys G, McCurdy DW, Offler CE (2007a) Deposition patterns of cellulose microfibrils in flange wall ingrowths of transfer cells indicate clear parallels with those of secondary wall thickenings. Funct Plant Biol 34:307–313

    Article  CAS  Google Scholar 

  • Talbot MJ, Wasteneys GO, Offler CE, McCurdy DW (2007b) Cellulose synthesis is required for deposition of reticulate wall ingrowths in transfer cells. Plant Cell Physiol 48:147–158

    Article  PubMed  CAS  Google Scholar 

  • Thiele K, Wanner G, Kindzierski V, Juergens G, Mayer U, Pachl F, Assaad FF (2009) The timely deposition of callose is essential for cytokinesis in Arabidopsis. Plant J 58:13–26

    Article  PubMed  CAS  Google Scholar 

  • Vaughn KC, Hoffman JC, Hahn MG, Staehelin LA (1996) The herbicide dichlobenil disrupts cell plate formation: immunogold characterization. Protoplasma 194:117–132

    Article  CAS  Google Scholar 

  • Vesk PA, Vesk M, Gunning BES (1996) Field emission scanning electron microscopy of microtubule arrays in higher plant cells. Protoplasma 195:168–182

    Article  Google Scholar 

  • Wiedemeier AMD, Judy-March JE, Hocart CH, Wasteneys GO, Williamson RE, Baskin TI (2002) Mutant alleles of Arabidopsis RADIALLY SWOLLEN 4 and 7 reduce growth anisotropy without altering the transverse orientation of cortical microtubules or cellulose microfibrils. Development 129:4821–4830

    PubMed  CAS  Google Scholar 

  • Williamson RE (1990) Alignment of cortical microtubules by anisotropic wall stresses. Aust J Plant Physiol 17:601–613

    Article  Google Scholar 

  • Wu HI, Spence RD, Sharpe PJH, Goeschl JD (1985) Cell wall elasticity. I. A critique of the bulk elastic modulus approach and an analysis using polymer elastic principles. Plant Cell Environ 8:563–570

    Article  PubMed  CAS  Google Scholar 

  • Zhao LM, Sack FD (1999) Ultrastructure of stomatal development in Arabidopsis (Brassicaceae) leaves. Am J Bot 86:929–939

    Article  PubMed  CAS  Google Scholar 

  • Zhong RQ, Burk DH, Morrison WH, Ye ZH (2002) A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14:3101–3117

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhong RQ, Burk DH, Nairn CJ, Wood-Jones A, Morrison WH, Ye ZH (2005) Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization. Plant Cell 17:1449–1466

    Article  PubMed Central  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (no. 298264-09) to G.O.W., a Fellowship to M.F. from the NSERC CREATE program Working on Walls, and the Canada Foundation for Innovation. We thank Derrick Horne and Kevin Hodgson from the UBC Bioimaging Facility for their expert advice.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Botany, University of British Columbia, 6270 University Blvd., Vancouver, B.C., V6T 1Z4, Canada

    Miki Fujita & Geoffrey O. Wasteneys

Authors
  1. Miki Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geoffrey O. Wasteneys
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Geoffrey O. Wasteneys.

Additional information

Handling Editor: David McCurdy

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

Movie showing abundant CSCs in cell cortex of elongating cells (MPG 96 kb)

Online Resource 2

Movie showing CSCs in vesicles and later accumulate at cell plate during cytokinesis (Left panel: Microtubules, Right panel: CSCs) (MPG 4578 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fujita, M., Wasteneys, G.O. A survey of cellulose microfibril patterns in dividing, expanding, and differentiating cells of Arabidopsis thaliana . Protoplasma 251, 687–698 (2014). https://doi.org/10.1007/s00709-013-0571-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-013-0571-2

Keywords

Search

Navigation